Regardless of whether a tree puts out flowers or unfolds its leaves first, new research suggests the time delay between the two phenological events has increased as global temperatures have risen.

Previous studies have found trees are putting out flowers and unfurling their leaves earlier as a result of global warming, but the latest research -- published Monday in the Journal of Ecology -- is the first to look at the time gap between the two

The unfolding of a tree's leaves mark the beginning of the year's growth cycles, while flowers signals the start of the reproduction cycle.

Between 1950 and 2013, the delay between these two annual events increased anywhere from 0.6 to 1.3 days per decade.

"The unequal advances of leaf unfolding and flowering may alter trees' partitioning of resources between growth and reproduction and could leave flowers or leaves vulnerable to late spring frost damage if they appear too early," Jian-Guo Huang, the corresponding author of the study and a researcher at the Chinese Academy of Sciences, said in a news release. "This could have impacts on tree species health and further affect ecosystem structure and function."

Scientists worry shifts in the timing of the two phenomena could put both leaves and flowers at risk of frost damage, as well as disrupt interactions with pollinators.

For the study, scientists utilized data from the Pan European Phenology network, which features data on the timing of leaf unfolding and flowering for a variety of tree species across Europe.

Researchers analyzed the timing of the two events for four species: horse chestnut, Scots pine, alder and ash trees. While most trees put out leaves first, alder and ash trees, which rely on the wind for pollination, open their flowers before putting out leaves, which could disrupt the breeze. For Scots pine trees, the separation of needles counts as the unfolding of leaves.

The data showed that for all four species, the two vital events are becoming increasingly disconnected. Researchers found the separation is widening more rapidly among trees in warmer areas of Europe.

"The timing of phenological events is very sensitive to environmental factors, with temperature being particularly important in temperate plants," said lead study author Qianqian Ma, researcher with the Chinese Academy of Sciences. "The changes in phenology we observed in our study may affect both growth and reproductive development in tree species and ultimately affect the ecosystem, nutrient cycles and carbon storage."

In followup studies, researchers hope to expand their analysis to including a wider variety of tree species, across Europe and elsewhere.

"Further studies that simultaneously monitor the timing of phenological events and the allocation of resources within plants are needed to better evaluate the consequences of altered phenology under climate warming," Jian-Guo Huang said.

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